Spatiotemporal analysis identifies ABF2 and ABF3 as key hubs of endodermal response to nitrate

Proc Natl Acad Sci U S A. 2022 Jan 25;119(4):e2107879119. doi: 10.1073/pnas.2107879119.

Abstract

Nitrate is a nutrient and a potent signal that impacts global gene expression in plants. However, the regulatory factors controlling temporal and cell type-specific nitrate responses remain largely unknown. We assayed nitrate-responsive transcriptome changes in five major root cell types of the Arabidopsis thaliana root as a function of time. We found that gene-expression response to nitrate is dynamic and highly localized and predicted cell type-specific transcription factor (TF)-target interactions. Among cell types, the endodermis stands out as having the largest and most connected nitrate-regulatory gene network. ABF2 and ABF3 are major hubs for transcriptional responses in the endodermis cell layer. We experimentally validated TF-target interactions for ABF2 and ABF3 by chromatin immunoprecipitation followed by sequencing and a cell-based system to detect TF regulation genome-wide. Validated targets of ABF2 and ABF3 account for more than 50% of the nitrate-responsive transcriptome in the endodermis. Moreover, ABF2 and ABF3 are involved in nitrate-induced lateral root growth. Our approach offers an unprecedented spatiotemporal resolution of the root response to nitrate and identifies important components of cell-specific gene regulatory networks.

Keywords: cell-specific; nitrate signaling; transcriptional regulation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / physiology
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Basic-Leucine Zipper Transcription Factors / genetics*
  • Basic-Leucine Zipper Transcription Factors / metabolism
  • Computational Biology / methods
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant*
  • Gene Ontology
  • Gene Regulatory Networks
  • Models, Biological
  • Nitrates / metabolism*
  • Organ Specificity / genetics
  • Plant Physiological Phenomena*
  • Plant Roots / physiology
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcriptome

Substances

  • ABF2 protein, Arabidopsis
  • ABF3 protein, Arabidopsis
  • Arabidopsis Proteins
  • Basic-Leucine Zipper Transcription Factors
  • DNA-Binding Proteins
  • Nitrates
  • Transcription Factors